The outdoor time in non-myopic children has decreased to that of myopic children during the SARS-CoV-2 pandemic

Objective: Low levels of outdoor activity are known to be an important risk factor for the development of myopia in schoolchildren. This study aimed to determine outdoor and near work patterns in Polish schoolchildren before and during school closure due to the SARS-CoV-2 pandemic. Methods: All children undergoing a routine pediatric examination in the Elbląg branch of the Hygeia Clinic, together with their parents, were asked to fill an anonymous questionnaire. The subject’s age, spherical equivalent (SE) refractive error, time spent outdoors, screen time and total near work in hours per day before and during the pandemic, were recorded. As substantial differences in physical activity by time of year were reported, activity patterns for June (summer) and December (winter) were recorded. Multiple logistic regression analysis was used to analyze the association between the presence of myopia and outdoor and total near work time at different timepoints. Results: A total of 61 schoolchildren aged 11.95 ± 2.74 (range 7 to 17) years were included in this study. The mean SE in the right eye was -1.78 ± 2.11 with 46% of the individuals (n=28) classified as myopic. Before the pandemic, higher time outdoors was associated with less myopic SE (OR=0.47, 95% Confidence Interval [CI] 0.24 to 0.93). During the pandemic, time outdoors among non-myopic children was similar to myopic children, both during winter and summer months (2.18 ± 1.81 vs. 1.89 ± 1.50; P=.51, and 3.47 ± 2.66 vs. 3.31 ± 1.65; P=.79 respectively). Time outdoors was not significantly associated with myopia during the pandemic (OR=1.17, 95% CI 0.64 to 2.14). Total near work was not associated with myopia at any time point. Conclusion: The long-term influence of the changing patterns of outdoor and near work on myopia prevalence and progression in our population is still to be established. Nevertheless, it is likely that the decrease of outdoor time may influence the rates of myopia in this region.


Introduction
Myopia is a common condition that develops in childhood and the prevalence of myopia among children worldwide varies from 0.7% among children aged 3-10 years in Saudi Arabia to 65.5% among teenagers aged 15 years in China [1][2][3]. Previously published studies from Poland revealed that the prevalence of myopia varied from 0.4% among children aged 7 years in the city of Poznan to 35.5% among children aged 17 years in Szczecin area, but those studies were performed at the beginning of the twenty-first century [3,4]. Myopia is an important public health problem, with nearly half of the world population being expected to have it in 2050 [1]. Progression to high myopia increases the risk of sight threatening complications in later adulthood, such as myopic macular degeneration. Low levels of outdoor activity are known to be an important risk factor for the development of myopia in schoolchildren [2,5].
The first cases of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) were reported in China in December 2019, while the global outbreak dates from the beginning of 2020, with the first European lockdowns in February 2020. The SARS-CoV-2 pandemic has led to significant changes in educational patterns, almost half of the world's students encountering partial or full-time school closure. During school closures, an increase in indoor time and near work activities, such as time spent on digital devices that are potential risk factors for myopia, were registered. Recent studies show an increased myopia prevalence and an accelerated myopic progression during the COVID-19 pandemic lockdowns in children and teenagers of different ethnic backgrounds [6][7][8][9][10][11]. However, the exact amount of near work, screen time and outdoor time during lockdown is not known in detail.
The aim of this study was to determine the outdoor and near work patterns in Polish schoolchildren before and during the pandemic.

Methods
All schoolchildren subscribed to the Elbląg branch of the Hygeia Clinic who underwent a routine medical examination from January to May 2021 were included in the study. Informed consent was obtained from all parents. Children with cataracts, glaucoma, having undergone previous ocular surgery, or suffering from any other ocular diseases were excluded. Together with their parents, the children were asked to fill in an anonymous questionnaire regarding their habits in terms of near work and outdoor time before and during the pandemic. The survey was designed to account for multiple activities and behavioral changes related to weather. Details regarding how many hours a child spent with a computer, phone, tablet, book or notebook and time outdoors were collected. Total near work time was defined as the sum of hours per day spent on the computer, phone, tablet, book and notebook. Outdoor time was defined as the sum of hours per day spent during outdoor activities, walking to and from the school, as well as outdoor activities during classes. As substantial differences in physical activity by time of year were reported, activity patterns for June (summer) and December (winter) were recorded (Fig. 1). Two sets of questions were prepared: one for activities before the pandemic and the second regarding their activities during the pandemic. The parents were also asked to state if their children were wearing glasses at the time of the visit and what was their refractive error in these glasses in diopters (sphere, cylinder and axis). Refractive error information was double-checked, if the parents were not certain about the refractive error of the child: (i) they were asked to contact their optician to obtain precise values; (ii) if they have priorly attended to the ophthalmic department of the clinic, these values were filled using prior medical records (iii) if the child was wearing glasses, they were measured with an automatic lensmeter by the nurse (CCQ-800, Yeasn Science & Technology Co. Ltd, Chongqing, China). The questionnaire was considered valid if all the fields, including refractive error, and time spent during the activities across several time points, were filled. The study adhered to the tenets of the Declaration of Helsinki and written consent was obtained for all parents and children provided assent. The study protocol was approved by the local bioethical committee (approval no. KB-37/21).

Data analysis
Myopia was defined as a myopic refractive spherical equivalent (SE) of 0.50 D or more. Hyperopia was defined as a hyperopic SE greater than +1.0 D. The spherical refractive error (E) was calculated as a sum of the sphere and half of the cylinder. The results were presented as the mean ± standard deviation. The normality of the data was assessed using the Kolmogorov-Smirnov test that showed a normal distribution. In normally distributed data, a paired sample two tailed t-test was performed Fig. 1 Study timeline. The study was conducted from January to May 2021. The children were asked to fill an anonymous questionnaire regarding their habits in terms of near work and outdoor time before (2019) and during the pandemic (2020). As substantial differences in physical activity by time of year were reported, patterns for June (summer) and December (winter) were recorded on compared datasets. Pearson correlation coefficients; values between 0 and 0.3 were considered weak positive, between 0.3 and 0.7 moderate positive, and between 0.7 and 1.0 strong positive linear relationships [12]. Multivariate logistic regression analysis was used to analyze the association between outdoor and total near work at different timepoints (before and during the pandemic) with the presence of myopia. A sample size of 54 eyes was estimated to detect a 1-hour difference in outdoor time, based on the estimation of the standard deviation for outdoor time of 2 hours, a power of 95% at a significant level of 5%. A p value less than .05 at a 95% confidence interval was considered as statistically significant. Statistical analysis was performed using Medcalc Software v. 14 (Medcalc Software ba, Ostend, Belgium) and IBM SPSS Statistics v. 28 (IBM Corporation, Armonk, NY, USA).

Results
The study enrolled 61 schoolchildren, 26 boys (42.6%) and 35 girls (57.4%). All questionnaires were considered valid, and none of the children was excluded from the study. The mean age of included children was 11.95 ± 2.74 years (range 7-17 years). The mean SE in the right eye was -1.78 ± 2.11 D. Twenty-eight children were classified as myopic (45.9%), two as hyperopes (3.3%) and thirty-one as emmetropes (50.8%). The results of the questionnaires are presented in Table 1. There was a significant seasonal variation for total near work before the pandemic compared to during the pandemic (P =.002 and P = .001, respectively), as well as for time outdoors before (2019) and during the pandemic (2020; P < .001 and p <.001, respectively). More importantly, there was a major change in the total near work during the pandemic, both in summer (P < .001) and in winter (P < .001). Time outdoors slightly decreased during the pandemic both in summer and in winter, but the difference was not significant (P =.38 and P = .05, respectively). All values are presented in hours per day. Girls tended to spend more time outdoors than boys, both before (3.00 ± 3.37 vs. 2.24 ± 1.10; P =.39, and 3.91 ± 2.49 vs. 3.40 ± 1.55; P =.37 for winter and summer months, respectively) and during the pandemic (2.13 ± 1.86 vs. 1.92 ± 1.36; P =.62, and 3.60 ± 2.49 vs. 3.10 ± 1.74; P =.39, for winter and summer months, respectively), but the difference was not statistically significant (Fig. 2).

Discussion
In this study, we found that before the pandemic myopic children were spending significantly less time outdoors than non-myopic children. This is concordant with what has been previously reported in other countries and the protective effect of time outdoors involves light-stimulated release of dopamine from the retina [13]. Importantly, during the pandemic, both myopic and non-myopic children spent similarly little time outdoors. This presumably led to an increase in the prevalence of myopia in that region. We also found that near work increased significantly during the pandemic in all children, and this increase was not different in myopic and nonmyopic children. Although near work has been shown to be a risk factor of developing myopia in schoolchildren [2], low levels of outdoor activity were shown to be more relevant [1,[3][4][5]13,14].
Due to the pandemic, schools were partially or fully closed ( Table 3) from March 2020, in several European countries. However, the level of restrictions in Poland can be considered as one of the greatest in Europe, the schools being closed for 43 weeks, while in Spain only for 13 weeks [15]. During the physical closing of schools, remote learning was implemented. The shift in near work habits, associated with the introduction of remote learning, was likely but has not been extensively evaluated. In Polish children included in this study, outdoor and near work patterns changed during the pandemic. Similar restrictions have been applied in the USA. In a recent study including 53 children (8.3 ± 2.4 years) from the USA, electronic device use increased significantly and outdoor time decreased during the pandemic in myopic children (n=14 myopes), but time spent on total near work (including reading and writing) was not significantly different [16]. In studies published before the SARS-CoV-2 pandemic, the rates of myopia in European countries have been moderate (Table 4) [2,17]. For example, in a Danish study by Lundberg et al.,17.9% of children (mean age of 15.4 ± 0.7 years) had much lower myopia than in several Asian countries [17]. Previous studies have shown that in Australia, European Caucasian children tend to spend more time outdoors than children of East Asian origin [18]. However, the children's pattern of activities become more myopigenic during the pandemic, and particularly associated with the introduction of remote learning. This shift may result in an increase of the prevalence of myopia and higher myopia progression in future.
In this study, it was noticeable that the most significant decrease in time outdoors influenced mainly non-myopic children. During the pandemic, their time outdoors became similar to that of myopic children. A previous study showed that in summer, during the pandemic, children from Houston, USA, spent approximately two hours less outdoors than before the pandemic [16]. In our cohort, this difference was much smaller, but still noticeable. Time outdoors is considered one of the major risk factors for myopia. In some countries, outdoor programs have been implemented as public health interventions to curb the myopia epidemic [19]. In a recent study, spending time outdoors in childhood was confirmed to be associated with a reduced risk (Odds ratio of 0.82) of myopia in adulthood [20]. Additionally, in a recent meta-analysis, spending time outdoors has been also shown to reduce axial elongation (mean difference=-0.03mm) [21]. Based on the results of several randomized controlled trials, it is recommended that children should spend at least two hours outdoors every day [22][23][24]. The study by Mirhajianmoghadam et al. conducted in the USA, reported similar results to those found in our study; during the COVID-19 pandemic, children demonstrated increased screen time and decreased outdoor activity [16]. Nevertheless, associations between near work and myopia have not been consistently observed. A study including children (n=414) aged 7 to 13 years, from the Collaborative Longitudinal Evaluation of Ethnicity and Refractive Error (CLEERE) study, showed that near work was not predictive of risk of juvenile onset myopia [25].
In this study, during the pandemic, screen time on smartphones increased nearly by half, while the computer screen time tripled. This was accompanied by a decrease of reading time with books and other non-digital reading materials. A recent meta-analysis has shown that smart device screen time alone (odds ratio 1.26 [95% CI: 1.0-1.6]) or in combination with computer use (odds ratio 1.77 [95% CI: 1.28-2.45]; I 2 =87%) was associated with myopia in children and young adults [26]. Importantly, the viewing distances associated with smart devices is smaller than other forms of near-vision work e.g., reading books, and the duration of exposure is usually longer [26]. Moreover, there is a growing body of literature showing that excessive use of digital media is associated not only with myopia, but also psychological, social and neurological adverse consequences [27]. The harming role of the change in visual habits should be considered when discussing potential school closures within the following years.  Limitations of our study included a small sample size. Additionally, refractive error was reported by parents and only assessed at a single point in time. Other limitations included the questionnaire collection of information about time spent during various activities during the pandemic, only collected at the clinic visit after the pandemic. Validity and reliability of the questionnaire were not tested and potential difficulties with recalling pre-pandemic patterns (almost a year later) may have induced potential biases. Similarly, we did not collect information about various weekday activities, but asked to estimate the average time spent in those activities. Still, one can consider that the behavior patterns did not differ that much between weekdays and weekends, particularly in the winter months, as low outdoor temperatures and precipitation could limit outdoor activities, but not school activities. Furthermore, the cross-sectional design of the study precluded any analysis of how the change in near work and outdoor may affect refractive error in future.

Conclusions
Outdoor and near work patterns in Polish children included in this study changed during the pandemic. In non-myopic children, before the pandemic outdoor time was higher than in myopic children. During the pandemic, time outdoors decreased and non-myopic children were spending similarly low time outdoors as myopic children. The long-term influence of the changing patterns of outdoor and near work on myopia prevalence and progression in our population is still to be established. Nevertheless, it is likely that the decrease of outdoor time may influence the rates of myopia in this region.